To investigate facial signaling, the best strategy is to focus on the visual features that are obviously adaptive in a species in which territoriality and ranking are prominent. What is adaptive in facial signaling is the correct reading of conspecifics' intentions at a safe distance. The signals must be robust if they are to be adaptive for both the emitter and the receiver. One cannot afford to hesitate whether an approaching outsider or a group member is friend or foe. But jumping too fast to the defensive in the presence of ambiguity can be equally ill-adaptive in species depending on cooperation which must have evolved unambiguous peace-making signals. Natural selection has favored signals based on the chromatic opposition: white versus any color of the spectrum. White ensures optimal reflectance even in reduced luminosity; the color upon which white patterns are produced by muscular contractions can vary indefinitely under other evolutionary forces, from camouflage to ostentatious handicap. Chemical and acoustic signaling is efficient in some environments, but, for open space species, chromatic signaling is the medium of choice, as it covers at the speed of light the distance required for fight or flight decisions. Tigers sport tuffs of white hairs on the back of their ears, which they twitch to produce white flashes toward approaching conspecifics to warn them of their alertness to the situation. Similar contrasts are exploited in the baring of teeth in canines and in the permanent status display of the tusks in elephants. The rich muscular system of the face in the primates makes it possible to vary the chromatic patterns, thus generating a range of leucosignals (from Greek leukos=brilliant white).
The human face makes constant use of the contrasts between the white patches of the sclera and the teeth, and the color of the facial skin (Bouissac Reference Bouissac, Cave, Guaitella and Santi2001; Reference Bouissac2005). These signals are well-defined, measurable, and subject to experimental manipulations. Muscular contractions create typical configurations of highly visible white patterns, which combine information pertaining to the gaze with information on the status of the jaws (relaxed vs. tense or clenched). The foldings of the skin can be relevant indicators, but can be only visible at a much closer range than the salient leucosignals and their well-defined morphologies. The range of data processed by Niedenthal et al. presupposes close range perception, while an inquiry into smiles as leucosignals is congruent with interaction at greater distances. The primate brain's face detectors are fast processors that must lead to instant decisions based on unambiguous signals (Tsao & Livingstone Reference Tsao and Livingstone2008).
It can be predicted, as Niedenthal et al. show, that leucosignals involve the amygdala, since previous evidence indicates that its activation correlates with processing social signals such as facial fear-generating information, including threats linked to social ranking (Buchanan et al. Reference Buchanan, Tranel, Adolphs, Whalen and Phelps2009, pp. 289–318). Neurons in the amygdala are indeed responsive to faces, particularly in a hierarchic group (Leonard et al. Reference Leonard, Rolls, Wilson and Baylis1985; Whalen et al. Reference Whalen, Davis, Oler, Kim, Kim, Neta, Whalen and Phelps2009), in which the white of the eyes and the teeth form distinct visual parameters (compare the ratio holding between sclera, iris, and eyelids in the fear face with the same ratio in the angry face). In all social species, the most dangerous enemies are conspecifics. Other predators of humans can be more easily manipulated or controlled, because their semiotic mismatch offers more windows of opportunity once it is deciphered. But in the human primates, peace-making is equally vital. It could thus also be predicted that the same neuronal systems would instantly switch from high alert to pleasure arousal or, at least, be processed by contiguous neuronal systems. Indeed, nothing is more threatening for a human than a new face on which intentions cannot be read. The production of friendly leucosignals may suddenly defuse the tense state of fight readiness and trigger the dopamine flow that stimulates the reward centers (Schultz Reference Schultz2007). All this is consistent with the data that are marshalled in Niedenthal et al.'s article without having to hypothetically construct the cognitive and emotional embodiment detailed by Niedenthal (Reference Niedenthal2007). This is not to deny that such embodiment may occur as a secondary effect with some adaptive consequences, but simply to point out that it is too costly in time and energy to be the primary source of vital decisions such as to trust, fight, or flee. Leucosignals can provide the fast and frugal information that triggers adaptive behavior without having to be emotionally processed.
Building from the basis of leucosignals, a scientific inquiry of the many facial configurations which are covered in English by the term smile would avoid getting conceptually entangled in the quagmire of semantic and literary interpretations, whether embodied or not. Niedenthal et al. rightly point out that Ekman (Reference Ekman2001) suggests that there might be as many as fifty kinds of smiles. The enigmatic or ironic smile (e.g., Mona Lisa with leucosignals reduced to the very minimum), the so-called Duchesne smile, the seductive smile (e.g., Barack Obama showing only his upper teeth), and the provocative triumphal smile in the face of adversity (e.g., Tony Blair showing both upper and lower teeth), to name only a few examples from contemporary icons, are most likely governed by neuro-behavioral systems that have evolved separately under a variety of selective constraints, and have in common only the fact that they end up on the display board of the face in the form of leucosignals whose meanings depend on the raw social context in which they occur. Whether they should all be labelled with the same term is highly questionable. Some are obviously gestures aimed at influencing conspecifics; others are probably mere leakages of a dopamine flooded inner state; and still others are likely the results of various interferences of any of these.
However, dealing with smiles from a purely biological evolutionary point of view definitely would miss the gene–culture coevolution, which cannot have failed to impact this most important tool of sociality. This latter dimension deserves more scrutiny than the lip service paid by Niedenthal et al. to the cross-cultural investigation of smiles.
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To investigate facial signaling, the best strategy is to focus on the visual features that are obviously adaptive in a species in which territoriality and ranking are prominent. What is adaptive in facial signaling is the correct reading of conspecifics' intentions at a safe distance. The signals must be robust if they are to be adaptive for both the emitter and the receiver. One cannot afford to hesitate whether an approaching outsider or a group member is friend or foe. But jumping too fast to the defensive in the presence of ambiguity can be equally ill-adaptive in species depending on cooperation which must have evolved unambiguous peace-making signals. Natural selection has favored signals based on the chromatic opposition: white versus any color of the spectrum. White ensures optimal reflectance even in reduced luminosity; the color upon which white patterns are produced by muscular contractions can vary indefinitely under other evolutionary forces, from camouflage to ostentatious handicap. Chemical and acoustic signaling is efficient in some environments, but, for open space species, chromatic signaling is the medium of choice, as it covers at the speed of light the distance required for fight or flight decisions. Tigers sport tuffs of white hairs on the back of their ears, which they twitch to produce white flashes toward approaching conspecifics to warn them of their alertness to the situation. Similar contrasts are exploited in the baring of teeth in canines and in the permanent status display of the tusks in elephants. The rich muscular system of the face in the primates makes it possible to vary the chromatic patterns, thus generating a range of leucosignals (from Greek leukos=brilliant white).
The human face makes constant use of the contrasts between the white patches of the sclera and the teeth, and the color of the facial skin (Bouissac Reference Bouissac, Cave, Guaitella and Santi2001; Reference Bouissac2005). These signals are well-defined, measurable, and subject to experimental manipulations. Muscular contractions create typical configurations of highly visible white patterns, which combine information pertaining to the gaze with information on the status of the jaws (relaxed vs. tense or clenched). The foldings of the skin can be relevant indicators, but can be only visible at a much closer range than the salient leucosignals and their well-defined morphologies. The range of data processed by Niedenthal et al. presupposes close range perception, while an inquiry into smiles as leucosignals is congruent with interaction at greater distances. The primate brain's face detectors are fast processors that must lead to instant decisions based on unambiguous signals (Tsao & Livingstone Reference Tsao and Livingstone2008).
It can be predicted, as Niedenthal et al. show, that leucosignals involve the amygdala, since previous evidence indicates that its activation correlates with processing social signals such as facial fear-generating information, including threats linked to social ranking (Buchanan et al. Reference Buchanan, Tranel, Adolphs, Whalen and Phelps2009, pp. 289–318). Neurons in the amygdala are indeed responsive to faces, particularly in a hierarchic group (Leonard et al. Reference Leonard, Rolls, Wilson and Baylis1985; Whalen et al. Reference Whalen, Davis, Oler, Kim, Kim, Neta, Whalen and Phelps2009), in which the white of the eyes and the teeth form distinct visual parameters (compare the ratio holding between sclera, iris, and eyelids in the fear face with the same ratio in the angry face). In all social species, the most dangerous enemies are conspecifics. Other predators of humans can be more easily manipulated or controlled, because their semiotic mismatch offers more windows of opportunity once it is deciphered. But in the human primates, peace-making is equally vital. It could thus also be predicted that the same neuronal systems would instantly switch from high alert to pleasure arousal or, at least, be processed by contiguous neuronal systems. Indeed, nothing is more threatening for a human than a new face on which intentions cannot be read. The production of friendly leucosignals may suddenly defuse the tense state of fight readiness and trigger the dopamine flow that stimulates the reward centers (Schultz Reference Schultz2007). All this is consistent with the data that are marshalled in Niedenthal et al.'s article without having to hypothetically construct the cognitive and emotional embodiment detailed by Niedenthal (Reference Niedenthal2007). This is not to deny that such embodiment may occur as a secondary effect with some adaptive consequences, but simply to point out that it is too costly in time and energy to be the primary source of vital decisions such as to trust, fight, or flee. Leucosignals can provide the fast and frugal information that triggers adaptive behavior without having to be emotionally processed.
Building from the basis of leucosignals, a scientific inquiry of the many facial configurations which are covered in English by the term smile would avoid getting conceptually entangled in the quagmire of semantic and literary interpretations, whether embodied or not. Niedenthal et al. rightly point out that Ekman (Reference Ekman2001) suggests that there might be as many as fifty kinds of smiles. The enigmatic or ironic smile (e.g., Mona Lisa with leucosignals reduced to the very minimum), the so-called Duchesne smile, the seductive smile (e.g., Barack Obama showing only his upper teeth), and the provocative triumphal smile in the face of adversity (e.g., Tony Blair showing both upper and lower teeth), to name only a few examples from contemporary icons, are most likely governed by neuro-behavioral systems that have evolved separately under a variety of selective constraints, and have in common only the fact that they end up on the display board of the face in the form of leucosignals whose meanings depend on the raw social context in which they occur. Whether they should all be labelled with the same term is highly questionable. Some are obviously gestures aimed at influencing conspecifics; others are probably mere leakages of a dopamine flooded inner state; and still others are likely the results of various interferences of any of these.
However, dealing with smiles from a purely biological evolutionary point of view definitely would miss the gene–culture coevolution, which cannot have failed to impact this most important tool of sociality. This latter dimension deserves more scrutiny than the lip service paid by Niedenthal et al. to the cross-cultural investigation of smiles.